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Current Protein and Peptide Science, 2014, 15, 351-362
351
Regulation of Photosynthetic Electron Transport and Photoinhibition
Thomas Roach1 and Anja Krieger-Liszkay2,*
1
Institut für Botanik, Leopold-Franzens-Universität-Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria;
Commissariat à l’Energie Atomique (CEA) Saclay, iBiTec-S, CNRS UMR 8221, Service de Bioénergétique, Biologie
Structurale et Mécanisme, 91191 Gif-sur-Yvette Cedex, France
2
Abstract: Photosynthetic organisms and isolated photosystems are of interest for technical applications. In nature, photosynthetic electron transport has to work efficiently in contrasting environments such as shade and full sunlight at noon.
Photosynthetic electron transport is regulated on many levels, starting with the energy transfer processes in antenna and
ending with how reducing power is ultimately partitioned. This review starts by explaining how light energy can be dissipated or distributed by the various mechanisms of non-photochemical quenching, including thermal dissipation and state
transitions, and how these processes influence photoinhibition of photosystem II (PSII). Furthermore, we will highlight
the importance of the various alternative electron transport pathways, including the use of oxygen as the terminal electron
acceptor and cyclic flow around photosystem I (PSI), the latter which seem particularly relevant to preventing photoinhibition of photosystem I. The control of excitation pressure in combination with the partitioning of reducing power influences the light-dependent formation of reactive oxygen species in PSII and in PSI, which may be a very important consideration to any artificial photosynthetic system or technical device using photosynthetic organisms.
Keywords: Electron transport, light stress, non-photochemical quenching, photoinhibition, photosynthesis, reactive oxygen
species, regulation.
INTRODUCTION
In oxygenic photosynthesis light energy, with the help of
light-harvesting antenna, is used to drive two specialized
complexes called photosystem I (PSI) and photosystem II
(PSII). The energy released from a captured photon triggers
charge separation in PSI and PSII reaction centres, and subsequent electron transfer reactions, enabling electrons and
protons to be taken from H2O and the release of O2. The released electrons are transported via a series of redox-active
co-factors to reduce a final electron acceptor, such as
NADP+. At the same time a proton gradient (pH) is generated across the thylakoid membrane that provides, together
with the electrochemical gradient (), the proton motive
force required for the synthesis of ATP. Charge separation
creates a positive charge at the donor side of the photosystems, which is reduced by plastocyanin in PSI and by electrons from the water-splitting complex in PSII. While the
absorption of light energy by antenna systems is highly efficient (i.e., extinction coefficient of chl: : approx. 105 M-1
cm-1), and helped by a broad range in absorption wavelengths by chlorophyll a, b and a number of carotenoid
molecules, energy is lost during charge separation, stabilization and onward electron transfer. In photosynthesis, further
energy is lost during CO2 fixation, especially under suboptimal conditions. In an optimal environmental setting, the
maximum conversion of solar energy to biomass is estimated
at 6%, but only for the most efficient plants [1, 2].
*Address correspondence to this author at the CEA Saclay, iBiTec-S, Bât.
532, 91191 Gif-sur-Yvette Cedex, France;
Tel: +33 16908 1803; Fax: +33 16908 8717;
E-mail: [email protected]
1875-5550/14 $58.00+.00
The reaction centres of PSI and PSII convert photon energy
into electrical potentials with very high efficiency (80 ± 15
% and 45 ± 10 %, respectively) [3] when measured on a microsecond timescale, making them highly attractive as potential photovoltaic devices [4, 5]. On longer timescales, however, the energy conversion efficiency is largely reduced to
about 40% for PSI [6]. Technical applications are increasingly exploiting the efficiency of photosynthesis for solidstate devices mimicking photovoltaic cells. Photo-electric
currents have been achieved with immobilized chloroplasts
[7], thylakoid membranes [8-10], PSII [11, 12] or PSI [1316] core complexes and isolated reaction centres [17-19].
One of the most promising current bio-photovoltaic without
using elaborate or expensive surface chemistries is a PSI
complex attached to a semiconductor, achieving a photocurrent density of 362 A/cm2 and 0.5 V [15]. Purified complexes [20], photosynthetic membranes [21-24] or whole
organisms [25-29] have also been placed on electrodes for
assembling biosensors (for review see [30, 31]), mainly for
the detection of pollutants, but also as components for future
H2 production devices [32]. As PSI has a higher efficiency
and is less prone to photoinhibion than PSII (see later), it
could be more suitable for biomimetic devices (for recent
reviews see [32-34]).
Natural photosynthesis is a highly regulated process.
Several mechanisms help to protect the photosystems against
light-induced damage (photoinhibition) when photon flux
densities exceed the photosynthetic capacity. Moreover, the
intensity when light becomes excess depends on the environment. Hence, in unfavourable conditions light saturation
occurs at lower intensities (Fig. 1). Excess energy that cannot
© 2014 Bentham Science Publishers
352 Current Protein and Peptide Science, 2014, Vol. 15, No. 4
be used to drive photosynthesis enhances the production of
reactive oxygen species (ROS) and induces photooxidative
damage. Although some regulatory mechanisms may only be
important in a living organism, energy dissipation and alternative electron pathways could be relevant for improving the
stability of technical devices based on the use of whole photosynthetic organisms like unicellular algae or of isolated
photosystems [35]. This review will cover the different levels that regulate photosynthesis in natural systems by using
examples from higher plants and the model green alga
Chlamydomonas reinhardtii. We start by covering the various pathways of light-induced production of ROS, major
sources of ROS in plants (for reviews see [36-40]), and then
cover how this relates to photoinhibition. The review continues with how excess energy can be dissipated to heat or distributed between the photosystems for protection, but also
for influencing the production ratio of ATP:NADPH. Furthermore, we will describe the various electron transport
pathways and highlight their importance, from linear to
pseudocyclic flow (also called the Mehler reaction) and cyclic, which seems particularly relevant to photoinhibition of
PSI. The control of excitation pressure in combination with
the partitioning of different electron transport pathways influences the light-dependent formation of ROS, thus is
paramount in controlling the stability and longevity of the
photosynthetic apparatus.
CO2 assimilation
Excess energy
Light intensity
Fig. (1). The light response curve of CO2 fixation. With increasing
absorbed quanta (dotted line), carbon assimilation eventually saturates and the difference between the two is excess energy. The level
when photosynthesis saturates is lowered under unfavourable conditions, as represented by the dashed line.
GENERATION OF REACTIVE OXYGEN SPECIES
AND PHOTOINHIBITION
Excitation of pigments and electron transfer reactions in
an oxygen-rich environment inevitably leads to photooxidative damage. This is visible to the eye by a bleaching of the
chlorophyll leading to pale green or even whitish leaves under extreme light conditions, especially when plants adapted
to shade are suddenly exposed to high light intensities.
Light-induced damage of the photosynthetic apparatus is
caused by excessive production of ROS such as singlet oxygen (1O2), superoxide (O2•-), hydrogen peroxide (H2O2) and
hydroxyl radicals (HO•) (Fig. 2).
Among the ROS, 1O2 and HO• are the most reactive species that are able to oxidize lipids, proteins and nucleic acids.
Although ROS are important signalling molecules in photosynthetic organisms, high production rates saturate antioxidant defences, lead to oxidative damage and ultimately reduce growth and plant fitness. The up regulation of antioxi-
Roach and Krieger-Liszkay
dant defences is part of an acclimation of photosynthetic organisms to very high light intensities [41]. Moreover, in nonliving devices the production of ROS for signalling purposes
is unnecessary, allowing ROS production to be minimised.
A
O2•-
O2•-
O2•-
cytb6f
PSI
1O
2
H 2O 2
PSII
H2O
B
SOD
O2•- + 2H+
APX PRX
H2O2
Fe2+/Cu+
•OH
+ OH-
Fe3+/Cu+2 O2•-
Fig. (2). Sites of reactive oxygen species (ROS) production at the
thylakoid membrane. [A] Singlet oxygen (1O2) production occurs
from charge recombination reactions in photosystem II (PSII),
whereas superoxide (O2•-) is predominantly produced by single
electron reductions of O2 at the acceptor side of photosystem I
(PSI). Other electron carriers, such as cytochrome b6f (Cyt b6f) may
also produce negligible amounts of O2•- or hydrogen peroxide
(H2O2). The dotted arrows represent electron flow. [B] The dismutation of O2•- to H2O2 is catalysed by superoxide dismutase (SOD),
which in the chloroplast is broken down by ascorbate peroxidase
(APX) and peroxiredoxins (PRX). In contact with Fe2+ or Cu+,
H2O2 can produce the hydroxyl radical (HO•) and Fe3+/Cu2+ can be
recycled with O2•-.
1
O2 is produced by the reaction of excited chlorophyll in
its triplet state (3Chl) with 3O2 (molecular oxygen is in a triplet state in its ground state). In the reaction centre of PSII,
3
Chl is generated by charge recombination of the primary
radical pair (P680+ Phe-), with pheophytin (Phe) being the
primary electron acceptor and P680 the primary chlorophyll
electron donor. When light absorption exceeds the capacity
of photosynthetic electron transport, the probability of 1O2
generation increases. The pathway of charge recombination
depends on the energetic of the electron acceptors of PSII
(for details see [42, 43]). Charge recombination between the
primary quinone electron acceptor (QA) and P680+ can proceed via an indirect pathway and the repopulation of the
primary radical pair or directly into the ground state of P680.
The indirect pathway leads to the formation of 3Chl and 1O2
while the direct pathway is safe (for a more detailed description see [44]). A regulation mechanism has been described
by which the yield of 1O2 production is lowered in PSII with
an inactive water-splitting complex. According to this
mechanism, 1O2 generation in PSII is controlled by a regulation of midpoint potential of QA. The yield of 1O2 formation
is lowered when QA is in its so-called high potential form,
i.e., when the midpoint redox potential of QA is shifted to a
more positive value. This shift in the midpoint potential allows a direct recombination of P680+QA- to its ground state
without repopulating the primary radical pair P680+Phe- [42,
44, 45]. PSII centres with high potential QA have been ob-
Regulation of Photosynthetic Electron Transport and Photoinhibition
served under different physiological conditions in vivo: 1) In
green algae prior to photoactivation (the light-dependent
assembly of the Mn cluster) [46], and 2) in leaves of higher
plants under high light conditions [40]. The dependence of
the amount of 1O2 generation in PSII upon the midpoint potential Q A has been demonstrated by electron paramagnetic
resonance (EPR) spectroscopy in vitro using a spin probe
[47] and in vivo by a specific fluorescence dye in Chlamydomonas [48, 49]. It has been shown that the yield of 1O2
generation correlates with the loss of the D1 protein, one of
the main subunits of the PSII reaction centre [50, 51]. Although chlorophyll-containing light hravesting complex
(LHC) of photosystems contain many more chlorophylls,
they are less susceptible to damage by 1O2. In native systems, these antennas are well protected against 1O2 formation
by nearby carotenoids, including xanthophylls, which efficiently quench 3 Chl [52, 53].
Photoinhibition and degradation of the D1 protein takes
place over a large range of light intensities, although a net loss
of PSII activity is only observed at high light intensities since
the repair of PSII is very efficient in vivo [54]. However, at
very low light intensities when the secondary PSII quinone
electron acceptor (QB) is only semi-reduced, photodamage and
D1 loss can also take place. For example, PSII photoinhibition
caused by charge recombination reactions and 1O2 generation
has been observed in green algae at very low light intensities
[55] and after excitation of PSII in isolated thylakoid membranes by single turnover flashes [56, 57]. It is not only the
midpoint potential of the redox couple QA/QA- that influences
the probability of the non-radiative pathway of charge recombination, but also the midpoint potential of the redox couple
Phe/Phe- [58]. Interestingly, cyanobacteria have two genes for
distinct D1 proteins, a main subunit of the PSII reaction centre, with different amino acids at position D1-130. Special D1E130 proteins are expressed only during high light conditions
[59], and are thought to shift the redox potential of Phe to enhance charge recombination via the safe non-radiative pathways, thereby lowering the yield of 1O2 generation [43]. Similar to the high light isoform of the D1 protein in cyanobacteria,
a glutamate occupies the position D1-130 in all higher plants
with known sequences. In Chlamydomonas, substitution of
alanine at D1-251 of the QB binding pocket to cysteine improved tolerance to cosmic radiation in space-flight and cell
survival after returning to earth [60]. PSII can undergo posttranslational modifications associated to stress protection and
repair. For example, the phosphorylation of the PSIIassociated chlorophyll-binding protein CP29 protects from
cold-stress [61]. Moreover, the D1 subunit is under a circadian-regulated phosphorylation pattern [62] and requires
dephosphorylation before it undergoes degradation [63].
Phosphorylation is also key to thylakoid membrane folding
enabling access of repair enzymes [64] and the migration of
photosystem antennas in state transitions, as discussed later.
For recent detailed reviews on photosynthesis-related phosphorylation readers are directed towards [65] and [66].
Beside 1O2 other ROS play an important role in lightinduced damage of the photosystems. Superoxide is mainly
generated at the acceptor side of PSI in the so-called Mehler
reaction [67, 68]. In this reaction, O2 is reduced by ferredoxin or by the PSI iron-sulphur acceptor Fx. In algae and
cyanobacteria reduction of O2 can be the dominant electron
Current Protein and Peptide Science, 2014, Vol. 15, No. 4
353
transport pathway [69], such as before the light-induced activation of the Calvin-Benson cycle [70], while in higher
plants its importance as alternative electron sink is thought to
be less important [71, 72]. It has been recently reported that
gymnosperms have an increased capacity of the Mehler reaction (about 10 % of the maximum electron flow) compared
to angiosperms, but only during dark to light transition before the Calvin cycle is active [73]. In angiosperms it is
thought that the importance of the Mehler reaction increases
under stress conditions, such as drought, when the CO 2
availability is limited by stomatal closure [71]. In addition it
has been reported that the photoperiod plays a role in the
partition between linear electron flow to NADP+ and Mehler
reaction [74]. Further investigations are needed to elucidate
the physiological importance of the Mehler reaction, if and
how it is regulated in vivo.
Besides being generated at the acceptor side of PSI, O2•can also be produced in vitro at the level of the cytochrome
b6f complex (cytb6f) [75] and at the acceptor side of PSII. In
addition, the cytochrome b559, an intrinsic protein subunit of
PSII can act, depending on its redox potential as an oxygen
reductase, as a superoxide reductase or as a superoxide oxidase [76]. However, the capacities of these pathways of O2
reduction seem to play only very minor roles in an intact,
functional electron transport chain in thylakoid membranes.
A major source of photosynthesis-associated ROS is the
H2O2 produced by photorespiration during the recycling of
bi-products of the oxygenase activity of RubisCO [77]. This
occurs outside the chloroplast in the peroxisome and will not
be discussed here. However, H2O2 is generated in isolated
chloroplasts, thylakoids and PSI or PSII preparations by the
dismutation of O2•-, either spontaneously or catalyzed by
superoxide dismutase (SOD). Small amounts of H2O2 can
also be generated directly by incomplete water splitting at
the donor side of PSII as has been shown in vitro using isolated PSII membranes [78]. Furthermore, it can be formed by
the reduction of O2•- by plastoquinol [79]. H2O2 itself is not
that toxic, but in the presence of transition metals, such as
Fe2+ or Cu+, it is converted to the highly reactive HO• radical
(Fig. 2). Apart from the Fenton reaction, HO • may also be
formed by the reduction of peroxide by metal centres coordinated to the proteins involved in electron transport.
In the intact chloroplasts, several enzymes are present
that detoxify ROS. O2•- is dismutated to H2O2 by SOD containing Cu and Zn (Cu/Zn-SOD) or Fe (Fe-SOD) as a cofactor. H2O2 is mainly detoxified by ascorbate peroxidase
(APX) [80] and by chloroplast-located peroxiredoxins (PRX)
[81]. While APX activity requires ascorbate, PRX activity is
dependent on re-reduction by thiol or thioredoxins. The
ascorbate (20-300 mM) and glutathione (GSH; 0.5 - 3.5 mM)
content of the chloroplast [82, 83] is sufficiently high enough
to enable a very efficient H2O2 detoxifying system [69]. Furthermore, thiols and thioredoxins are substrates for glutathione peroxidases and glutathione-s-transferases, which
are important in detoxifying reactive lipid species formed by
1
O2 [84, 85]. 1O2 can be scavenged by tocopherol, plastoquinone, carotenoids and by ascorbate [86-88]. Despite ascorbate, these scavengers are present in isolated systems and
will help to protect the photosystems in the light. However,
they have limited capacity because regeneration cannot take
354 Current Protein and Peptide Science, 2014, Vol. 15, No. 4
place and after a given time they become exhausted. The
addition of catalase, a non-chloroplast located enzyme, increased the efficiency and stability of thylakoid bioelectrodes [8] confirming that H2O2 production can be an
issue in artificial devices.
It is accepted by the majority of researchers that ROS directly damage photosystems with PSII being more vulnerable against oxidative damage than PSI. However, some researchers have suggested that the repair mechanism of the
D1 protein is solely damaged by ROS, and not the PSII reaction centre itself (see Special Issue Physiologia Plantarum
2011 for the current debate). In vivo, the repair of PSII is so
efficient that damage is only transitory [54]. Addition of
methylviologen to isolated thylakoids, which enhances O2•at the acceptor side of PSI, still led to greater inhibition of
PSII than PSI [89], showing that PSII is much more susceptible to ROS-induced damage than PSI, even when the site of
production is located at PSI. It is intriguing that the D1 reaction centre at the heart of PSII photoinhibiton has remained
highly susceptible to photo-damage in all oxygenic photosynthetic organisms and at all light intensities. Despite the
apparent wastefulness of PSII photoinhibition, it can also be
regarded as a regulatory mechanism of photosynthesis, since
it lowers linear electron transport under excess light conditions and may thereby prevent photoinhibition of PSI [90].
Photoinhibition of PSI has a higher impact on the performance of the photosynthetic apparatus since no efficient repair
cycle exists [90].
REGULATION OF LIGHT HARVESTING
What makes photosynthesis remarkable is that it efficiently functions under highly fluctuating photon flux densities, under environmental constraints and in accordance with
the metabolic demands of the organism. Photoregulation is
coordinated at multiple levels; At the pigment and protein
levels via energy-transfer processes involving carotenoids
and chlorophylls, at the membrane and cellular levels with
supramolecular organization in the thylakoid membrane, at
the cellular level by chloroplast relocation and at the organism level including heliotropism of plants and phototaxis of
microorganisms. Within the thylakoid membrane, light harvesting complexes facilitate in capturing light energy and its
transfer to the reaction centres for charge separation. This
partitioning between light harvesting and reaction centres
provides an opportunity in regulating how much and to
which reaction centre energy is delivered to, thereby preventing excessive excitation, ROS production and the costs associated with photoinhibitory damage. Collectively, this plethora of regulatory mechanisms controlling light energy in
intact organism is known as non-photochemical quenching
(NPQ), due to their detection by measurements of chlorophyll fluorescence quenching that are distinct from photochemical quenching (i.e., use of the captured light energy in
chemical reactions such as CO2 fixation). For a complete
guide on chlorophyll measurements of photosynthetic efficiency readers are directed to [91]. There are three components to NPQ; 1) dissipation of excess light energy in antenna to heat before it reaches the reaction centre (qE), 2)
state transitions where light adsorption is balanced between
the photosystems by movement of antenna (qT) and 3) ‘short
term’ photoinhibition of PSII (qI), which recovers slower
Roach and Krieger-Liszkay
than qE or qT [92, 93]. As discussed below, qT and qE are
governed by the plastoquinone (PQ) pool redox state and the
thylakoid proton-motive force, respectively, which makes
photosynthesis a highly efficient self-regulated process. For
a comprehensive review on how photosynthetic organisms
respond to excess light see [94].
THE QE COMPONENT OF NPQ
The qE component of NPQ, where light energy is
dissipated before reaching the reaction centres, has been
assigned to a synergistic action of the pH since a low pH in
the thylakoid lumen activates the xanthophylls cycle and
leads to protonation of luminal residues of proteins such as
PsbS and LhcSR3 that reduce energy transfer from the antenna to the PSII reaction centre (Fig. 3). In the xanthophyll
cycle, the low pH activates a de-epoxidation of violaxanthin
to zeaxanthin and requires minutes to hours to become fully
activated [95, 96], but zeaxanthin can temporarily remain
active after the loss of the pH [93]. Lutein is another xanthophyll implicated in qE and protection from high light in
both Arabidopsis and Chlamydomonas [52, 97]. Another
pH-dependent component of qE is protonation of light harvesting complexes (LHC) and an LHC-type protein, which
rapidly induces NPQ within seconds [98]. In higher plants
this trans-membrane LHC-type protein is PsbS [99], whereas
in green algae (e.g., Chlamydomonas) it is LhcSR3 [100].
Differences between the proteins include PsbS being constitutively expressed and not binding pigments, whereas LhcSR3
is highly inducible by excess light and binds chlorophyll and
carotenoids [101]. Moreover, the mechanism of LhcSR3 is
less dynamic than PsbS and leads to quenching even in low
light, which is perhaps why LhcSR3 is a high light-inducible
protein [101, 102]. Evidence suggests the switch from
LhcSR3 to PsbS happened when organisms colonised the
land and was likely associated with the extra stresses associated with terrestrial life [103]. Mosses can contain both proteins as has been shown for Physcomitrella patens [104] and
Rhytidium rugusum (data not shown). Regardless, mutants of
Arabidopsis or Chlamydomonas deficient in either PsbS or
LhcSR3, both referred to as npq4, have retarded abilities to
dissipate excess energy and show sensitivity to high or naturally fluctuating light [100, 105]. The aggregation of LHC II
trimers and detachment from PSII is also observed during qE
induction [106]. Due to the influence of pH on qE, a regulation of ATP synthase activity, which uses the pH to produce
ATP also influences NPQ [107], possibly through thioredoxin-mediated redox control, but this has yet to be confirmed [108]. Recommended introductory reviews to qE are
[102, 109] for model plants and [110] in other plants, but also
see [52, 111] for further debate.
We have recently shown in vitro using Arabidopsis chloroplasts that 1O2 production is influenced by the presence or
absence of PsbS-dependent NPQ capacity [112]. Other
markers of 1O2 production are the oxidation of -carotene
inside the reaction centre and of prenyllipids such as tocopherol and plastoquinone [86]. It has also been reported
that -carotene is more oxidised in Arabidopsis npq4 than
wild-type following excess light stress, confirming qE protects against reaction centre damage by 1O2 [113]. In addition to qE, other mechanisms of energy dissipation operate in
specialised situations. For example, a light- and nigericin-
Regulation of Photosynthetic Electron Transport and Photoinhibition
insensitive activation of the xanthophyll cycle has been
shown in a desiccation-tolerant fern and in lichens [114].
Moreover, an induction of non-radiative charge recombinations in PSII (see above) occurs in cyanobacterial desert
crusts in response to high light, avoiding the formation of
3
Chl and associated 1O2 [115]. Although NPQ is essential to
the contribution of desiccation tolerance [116], the contribution of the xanthophyll cycle to NPQ is not always supported, indicating that other mechanisms, such as chlorophyll
cations that are very efficient quenchers [117], are responsible for the desiccation-induced NPQ [118]. However, xanthophylls may play other roles in protection from excess
light due to their efficient ability to scavenge ROS, such as
zeaxanthin protecting from 1O2 [119, 120] and neoxanthin
from O2•- [121]. In cyanobacteria, a different type of qE has
been described which relies on the light-induced conversion
of the Orange-Carotenoid-Protein (OCP) to its active red
form that quenches fluorescence (for review see [122]).
qE component of NPQ
Current Protein and Peptide Science, 2014, Vol. 15, No. 4
Consequently LHCII migrates back to PSII, referred to as
‘state 1’. State transitions play a minor role in higher plants
while they are highly important in green algae. In Arabidopsis, where only up to 15-20% of LHCII can be mobilised
[124, 125], state transitions are important in acclimating to
changing light intensities [126]. However, in Chlamydomonas 70- 80% of can disassociates from PSII [127], but
only 20 % associates to PSI [127, 165]. It had been accepted
in the literature for a long time that in Chlamydomonas the
transition from state 1 to 2 is accompanied by a switch from
linear to cyclic electron flow [128]. However, it has recently
been demonstrated that this is not necessarily the case [129].
Although both state transitions and cyclic electron flow are
induced by reducing conditions, the migration of LHCII to
PSI is not a prerequisite for the induction of cyclic electron
flow [129].
qT component of NPQ
LHCII
Light
Heat
CO2
assimilation
LHCII
High
light
Fig. (3). Mitigating excess light via the qE component of nonphotochemical quenching. With increasing light intensities, the
light-dependent production of a proton gradient across the thylakoid
membrane induces two mechanisms that dissipate excess light energy to heat before it reaches the photosystem II reaction centre.
Acidification of the lumen 1) enhances the enzymatic conversion of
violaxanthin to antheraxanthin and zeaxanthin, and 2) protonates
key residues of light harvesting complex II and PsbS (vascular
plants) or LhcSR3 (green algae), which together participate in the
dissipation of excess energy at the level of the PSII antenna preventing excess light from causing damage.
LHCII
e‐
PQ
PQH2
e‐
LHCII
e‐ e
PQH2 Cyt
PQH2 b6f
e‐e‐
[A]
Light intensity
PsbS/LhcSR3/LHC protonation
Zeaxanthin formation
355
PSII
Cyt
b6f
PSI
e‐
State 1
‐
[B]
PSII
[C]
State
2
PSI
e‐
Cyt b6f and LHCII migration
e‐
e‐
Cyt
PQ
PSI
PSII PQH2
b6f
e‐
e‐
LHCII
Fig. (4). Balancing light absorption by the photosystems via state
transitions poised by the redox state of the plastoquinone pool. [A]
Under moderate light, the redox state of the plastoquinone pool
(PQ/PQH2) remains largely oxidised allowing linear electron flow,
and the majority of light harvesting complex II (LHCII) is at PSII
(state 1). [B] If PSII becomes over-excited relative to PSI, the PQ
pool becomes over-reduced, favouring the binding of PQH2 to the
Qo site of the cytochrome b6f complex (cytb6f), which induces a
kinase to phosphorylate LHCII and the movable part of LHCII migrates to PSI. [C] The migration of LHCII to PSI (state 2) reduces
excitation pressure at PSII lowering linear electron transport so that
the PQ pool becomes re-oxidised.
THE QT COMPONENT OF NPQ
Another light-inducible response, the so-called state transitions, influences excitation delivery to the photosystems.
Light Harvesting Complex II (LHCII) can migrate to change
the energy deliverance to PSII or PSI. Moreover, the movement of LHCII away from PSII relieves excitation pressure
[123]. The migration of LHCII is under governance of the
plastoquinone pool redox state, and therefore, the relative
activities of PSII and PSI. Under high PSII activity and a
reduced plastoquinone pool, plastoquinol binds to the Qo site
of the cytb6f, which activates protein kinase STN7 to phosphorylate LHCII [124]. This is a pre-requisite for its movement to PSI and the induction of ‘state 2’ (Fig. 4). A more
oxidised plastoquinone pool leads to the dissociation of plastoquinol from the Qo site of cytb6f, thereby deactivating the
kinase and activating a phosphatase (as reviewed by [65]).
The activation of high light responses are upregulated at
different times and at different intensities depending upon
the organism, presumably to address the different demands
and adjustments. The fasted responses are qE (first minutes
upon exposure to high light, followed by state transitions
(qT) and finally leading to photoinhibition of PSII (qI). Although each mechanism has unique functions they also possess overlapping protective roles.
REGULATION OF THE ELECTRON TRANSPORT
CHAIN
Beside the regulation of the amount and distribution of
light energy to the reaction centres, the activity of the electron transport chain can be down regulated at different sites.
The size of the pH is the most important component that
356 Current Protein and Peptide Science, 2014, Vol. 15, No. 4
not only controls qE (see above), but also regulates electron
transport at the level of the cytb6f and at the donor side of
PSII. A decreased luminal pH limits electron transport by
slowing the activity of the cytb6f, a regulation mechanism
called “photosynthetic control” [130, 131]. The lumen pH in
Arabidopsis leaves under ambient CO2 was estimated to
range from approximately pH 7.5 to 6.5 under weak and
saturating light, respectively [132]. These moderate pH values in the lumen allow regulation at the antenna level via qE
and via electron transport through the cytb6f, as well as preventing acid-induced damages. The pH value for zeaxanthin
accumulation and PsbS protonation was estimated to be
about 6.8 [132]. When net ATP synthesis is zero, the pH in
the lumen can decrease as low as pH 5.2 (for review see
[130], a pH at which the water-splitting activity and the reduction kinetics of P680+ start to be slowed down [133]. Below pH 5.5, Ca2+, an obligatory co-factor of the watersplitting complex is reversibly removed, evoking a shift of
QA to the high potential form [134] and protecting PSII
against 1O2 generation (see above).
Beside processes that are regulated by the luminal pH, alternative pathways of photosynthetic electron transport can
release the pressure from the electron transport chain and
prevent photoinhibtion. Under conditions of limiting light
and no limitation on the electron acceptor side (i.e., sufficient CO2), linear electron transport is dominating and electrons released from splitting H2O in PSII are used by PSI to
reduce electron acceptors such as NADP+. As electron acceptors become limited (i.e., low CO2 that limits NADPH
oxidation for carbon assimilation), pseudocyclic electron
flow / Mehler reaction (where O2 is the electron acceptor)
and cyclic electron flow are increasingly able to compete for
reducing power (Fig. 5). In cyclic electron flow the reducing
power is not from PSII, but instead recycled back from PSI
into the plastoquinone pool and via cytb6f. This occurs directly via ferredoxin and other proteins, such as PGR5 [135]
and PGRL1 [136, 137], or via NAD(P)H dehydrogenases
(NDH) [138]. As the reinvested reducing power of cyclic
electron flow passes through the Q-cycle of cytb6f, the accompanied proton transport from stroma to lumen facilitates
the formation of pH, and hence, ATP production. For photosynthetic organisms switching between cyclic and noncyclic pathways provides a degree of flexibility in the ratio
of ATP and NAPDH production to meet metabolic needs
[139, 140]. This is particularly important in ATP-expensive
photosynthesis, such as CAM plants and in the bundle sheath
cells of C4 plants, which both require a higher ATP:NADPH
ratio for CO2 fixation than C3 photosynthesis. Furthermore,
cyclic flow is enhanced when CO2 becomes limiting in both
higher plants [141] and Chlamydomonas, the latter which has
a high ATP demand under CO2 limitation because CO2concentrating mechanisms operate at the expense of ATP
[142]. Cyclic electron flow is clearly linked to stress, but the
exact regulatory mechanism that switches it on is still unknown. A joint PSI-cytb6f supercomplex for cyclic electron
flow has been demonstrated biochemically to be formed in
Chlamydomonas [129, 143], but not yet in higher plants. The
NAD(P)H dehydrogenase (NDH) route in Chlamydomonas
is achieved by a monomeric protein called Nda2 [144], while
in higher plants it is achieved by the NDH complex [145,
146]. Both can operate in the dark with non-photosynthetic
Roach and Krieger-Liszkay
supplies of NAD(P)H. In Arabidopsis, at least, both the
PGR5/PGRL1-dependent and the NDH-dependent cyclic
pathways seem to be under redox regulation by thioredoxin
m4 [147], while the PSI-cytb6f supercomplex is Ca2+dependent in Chlamydomonas [136].
As discussed above, cyclic electron transport is enhanced
to support the production of a pH under conditions that
limit carbon assimilation, including environmental stress.
Thus it allows ATP generation without the net formation of
reductants, such as reduced Ferredoxin or NADPH. The
exclusion of linear electron flow also limits the Mehler
reaction and O2•- generation. Moreover, cyclic electron flow
protects against photodamage of PSI since it keeps the
acceptor side oxidized [90, 112, 135, 148, 149].
In addition to partitioning between linear electron flow,
cyclic flow and Mehler reaction (Fig. 5), the plastid terminal
oxidase (PTOX), which directly oxidises plastoquinol while
reducing O2 to H2O, has been proposed to act as a safety
valve and to avoid photo-oxidative damage [150]. PTOX
activity may also enhance the formation of a pH, as demonstrated in marine organisms that survive in iron-depleted
waters. Here, the cost of building iron-rich PSI is very high,
but organisms can operate with PSII activity alone [151]. In
alpine plants the level of PTOX protein is elevated, which
may be linked to their ability to tolerate harsh conditions like
very high irradiation at low temperatures [150, 152]. In
agreement with this, PTOX levels are increased in plants
exposed to extreme temperatures [153, 154] or to high salinity [155]. In Chlamydomas two isoforms of PTOX exist,
PTOX and PTOX2. PTOX2 has been shown to keep the PQ
pool oxidized in the dark [156]. However, in other model
plants such as Arabidopsis thaliana, Nicotiana tabacum and
Solanum lycopersicum grown under standard conditions, the
role of PTOX in mature leaves is less clear. Overexpression
of PTOX did not protect plants from photoinhibition [157]
but actually enhanced it in some circumstances [158, 159].
Recent evidence indicates that PTOX rather modulates the
balance between linear and cyclic flow than acting as a
safety valve [160] since the capacity of electron flow via
PTOX has been measured to be very limited in S. lycopersicum leaves [157]. Further investigations are needed to
show the importance of PTOX as a safety valve under stress
conditions.
In summary, the competition for absorbed quanta by alternative electron flows becomes important when the electron acceptor NADP+ is limited. These electron flows include cyclic flow around PSI, the Mehler reaction and PTOX
activity. Not only does this enable metabolic adjustment
through regulating ATP:NADPH ratios, but also releases
reducing pressure off the electron transport chain, lowering
incidences of charge recombination and preventing 1O2 production (see above). Hence, the incorporation of a regulatory
mechanism to prevent over-reduction of charge carriers
could also be attractive to artificial systems that may suffer
damage under high loads.
COST-BENEFIT
MECHANISMS
RATIO
OF
REGULATORY
An obvious cost of photoregulatory processes is the loss
in efficiency in photosynthetic yield. A delay in recovery of
Regulation of Photosynthetic Electron Transport and Photoinhibition
NPQ from the residual presence of zeaxanthin after high
light treatment [93] may have high costs in carbon assimilation of agricultural plants [161]. In the non-native setting
of agriculture that strives for maximum growth rates, the
protection afforded by NPQ may well be, at times, too conservative. Therefore, opportunities for genetically manipulating light harvesting mechanisms for optimising yields
may exist [162]. However, photoregulation prevents photoinhibition, which itself is costly in energetics and resources for repairing damaged reaction centres as well as in
the photosynthesis forgone during repair (reviewed by
[163]). Other protective expenses to photosynthetic organisms are the investment in antioxidants, such as ascorbate,
that require complex biosynthetic pathways and reductants
with other enzymes to recycle their activity. Therefore, the
cost-benefit ratio of photoregulation versus photoinhibition
is extremely complex, especially considering an ecological
setting with unpredictable resource availability. As mentioned above, photoinhibition itself is a regulatory process
of biological photosystems that can rapidly repair themselves. This brings into question the perhaps impossible
task of increasing the longevity of isolated reaction centres
in biomimetic systems, but the incorporation of exogenous
antioxidants can help [8].
Electron transport pathways
[A]
PSII
cytb6f
PSI
NADP+
Linear
PQH2
[B]
H2O
-ATP
-NADPH2
O2
Pseudocylcic
PQH2
-ATP (O2•-)
H2O
pgr5/pgrl1
[C]
NDH
PQH2
Cyclic
-ATP
Fig. (5). Photosynthetic electron transport pathways. In linear
electron flow [A] electrons released by water-splitting in photosystem II (PSII) reduce plastoquinone to plastoquinol (PQH2 ),
which migrates to the cytochrome b6 f complex (cytb6 f). Plastoquinol is oxidized by the cytb6f and protons are released into the
thylakoid lumen. Electrons are transported to plastocyanin (PC),
which is the electron donor to photosystem I (PSI). At the acceptor side of PSI electrons are donated to NADP+. Alternatively,
PSI can reduce O2 producing O2•- (Mehler reaction or pseudocyclic flow) [B]. In cyclic electron flow [C] the reducing power from
PSI is re-invested back into the electron transport chain via
NADPH dehydrogenase (NDH), which reduces the plastoquinone
pool, or via a pgr5/pgrl1 protein complex to cytb6 f . All electron
flows permit the generation of a thylakoid proton gradient for the
generation of ATP, whereas only linear flow produces NADPH/H
for carbon assimilation.
Current Protein and Peptide Science, 2014, Vol. 15, No. 4
357
USE OF REGULATORY MECHANISMS FOR TECHNICAL EXPLOITATION
The question arises as to what we can learn from the
regulatory mechanisms of natural photosynthesis for using
photosynthetic machinery in technical applications. First,
one has to distinguish between technical applications that are
either based on exploiting whole organisms as biosensors or
using isolated complexes enriched with photosynthetic complexes. Inhibition of the photosynthetic electron transport in
whole organisms is easily detectable by monitoring chlorophyll fluorescence and is used to detect heavy metal or herbicide pollution in water. Recent exploits using laser printing
have achieved greater contact of electrodes with whole cells
[164] or thylakoids [23], increasing efficiency of charge
transfer and sensitivity of biosensors to the nM range [23,
25]. In an intact organism all natural regulatory mechanism
are present and can be activated depending on the environmental conditions. To allow a long-term use of a biosensor
based on intact organisms it has to be ensured that enough
nutrients and CO2 are available and that waste is removed
when intact organisms are embedded into a matrix for the
technical application.
Regarding isolated systems, PSII complexes or PSIIenriched membrane fragments have already been tested as
sensors to detect herbicides. Instead of using active PSII, with
the highly vulnerable water-splitting complex, it may be interesting to use PSII with an inactivated donor side. Inactivation
of the donor side leads to the shift of the midpoint potential of
QA to the high potential form as described above. PSII with
high potential QA is protected against damage by 1O2. Herbicides bind efficiently to these modified PSII and herbicide
binding could be detected by either measuring thermoluminescence or herbicide-induced changes in the decay kinetics of
chlorophyll fluorescence. Isolated photosynthetic systems may
well be devoid of metabolic control required in whole organisms in responding to changes in the environments like fluctuating light, but in an outside environment they will still be
subjected to highly variable conditions of temperature and
light intensity, affecting efficiency and performance. Therefore, when isolated thylakoid membranes or isolated PSI
preparations will be used in a technical device, it may be useful to add a safety valve in analogy to the PTOX or the Mehler
reaction present in the natural system. This safety valve should
only operate when PSI (or both photosystems in case of thylakoids) becomes saturated. To design such a safety valve, a
better understanding of the regulation of the Mehler reaction
and of PTOX are first needed before reasonable suggestion
can be made based on physiologically relevant protection
mechanisms. As the field of bio-sensors and transducers is
only in its infancy, we can expect great advances when technological advances are coupled with an enhanced understanding of photosynthesis and its control.
CONFLICT OF INTEREST
The authors confirm that this article content has no conflicts of interest.
ACKNOWLEDGEMENTS
We would like to thank José Ignacio García-Plazaola,
University of the Basque Country, Spain, and Kathleen
358 Current Protein and Peptide Science, 2014, Vol. 15, No. 4
Roach and Krieger-Liszkay
Feilke, CEA Saclay, for critical reading of the manuscript.
TR was supported by EU FP7 Marie Curie Initial Training
Network HARVEST (FP7 project no. 238017). This publication is supported by Grant of COST Action TD1102. COST
(European Cooperation in Science and Technology) is
Europe’s longest-running intergovernmental framework for
cooperation in science and technology funding cooperative
scientific projects called 'COST Actions'. With a successful
history of implementing scientific networking projects for
over 40 years, COST offers scientists the opportunity to embark upon bottom-up, multidisciplinary and collaborative
networks across all science and technology domains. For
more information about COST, please visit www.cost.eu.
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